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Diffuse idiopathic skeletal hyperostosis in Meroitic Nubians from Semna South Sudan.

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Diffuse Idiopathic Skeletal Hyperostosis in Meroitic Nubians From
Semna South, Sudan
Department of Anthropology and Ethnic Studies, University of Nevada,
Las Vegas, Los Vegas, Nevada 89154-5012 and Smithsonian Institution,
Department of Anthropology, National Museum of Natural History,
Smithsonian Institution, Washington, D.C. 20560 (B.T.A.1; Department of
Anthropology, Arizona State University, Tempe, Arizona 85287-2402
(C.F.M.1;Arthritis Center of Northeast Ohio, Northeast Ohio Universities,
College of Medicine, Youngstown, Ohio 44512 (B.M.R.)
Vertebral column
The paleopathological study of human osteological remains
from the site of Semna South, of northern Sudan, revealed that about thirteen
percent of this ancient Nubian population had diffuse idiopathic skeletal
hyperostosis (DISH). As in modern cases, males were more affected than
females. Two thousand years ago, ancient Nubian males had the same spinal
problems elderly men have today. o 1993 Wiley-Liss, Inc.
This paper summarizes paleopathological
research undertaken on a Nubian skeletal
collection to search for early evidence of diffuse idiopathic skeletal hyperostosis (DISH)
in Africa. DISH is a common skeletal abnormality, affecting 20-27% of men over 50
years of age (Forestier and Lagier, 1971;
Resnick et al., 1978; Rothschild, 1988;
Rothschild and Woods, 1991).DISH does not
cripple the individual; thus, some scholars
do not consider it a disease, but rather an
anomaly of aging or a special skeletal phenomenon (Resnick et al., 1978; Resnick and
Niwayama, 1976; Rothschild, 1988). From
the systematic clinical studies done by
Forestier and Rotes-Querol (1950) and
Forestier et al. (1956), the first diagnostic
criteria were derived. As Forestier and
Rotes-Querol used the term “ankylosing hyperostosis” to designate a specific type of
spinal anomaly which was clearly distinct
from ankylosing spondylitis, the phenomenon is also referred to as Forestier’s disease
or as Forestier and Rotes-Querol disease.
DISH has gone by various names in the past
(Table 1). In 1975, Resnick and his co-workers coined the term “diffuseidiopathic skele0 1993 WILEY-LISS, INC.
tal hyperostosis” (DISH) to emphasize that
extra spinal manifestations, enthesis ossifications, are also common. The acronym
DISH is currently preferred over ankylosing
The etiology of DISH is unknown. DISH
has a distinctive morphology that differentiates it from other rheumatic disorders.
DISH is typified by ossification of the anterior longitudinal ligament, especially along
the right anterolateral aspect of the thoracic
vertebrae (Fig. 1). DISH is easily recognizable in a lateral radiographic view of the
spine. The outgrowths appear as a dense
and continuous line of bumps, or as a “candle flame.” In the bare bone this condition
can be observed as a flowing ossification
Received for publication June 25,1992; accepted May 19,1993.
Address reprint requests to Dr. Bernard0 T. Arriaza, Department of Anthropology and Ethnic Studies, University of Nevada,
Las Vegas, 4505 Maryland Parkway, Las Vegas, Nevada 891545012.
the sacroiliacjoints in DISH are not fused as
in ankylosing spondylitis. Individuals with
Forestier’s disease
DISH keep most of their back flexibility,
Ankylosing hyperostosis
whereas those with ankylosing spondylitis
Moniliform hyperostosis
do not. Back flexibility is possible in paHyperostosis of the spine
Spondylosis hyperostotica
tients with DISH because most anterior
SDondvlitis ossificans kamentosa
flexion occurs at the lumbar segment and
Senile“anky1osinghyper&& of the spine
Ankylosing hyperostosis of Forestier and Rotes-Querol
DISH typically affects the thoracic segment
instead. In contrast, in patients with anky‘After: Resnick e t al. (1978);Utsinger (1984).
losing spondylitis, back flexion is restricted
due to fusion of the lumbar vertebral bodies
and their apophyseal joints. Vertebral squaring, which typifies ankylosing spondylitis,
does not occur in DISH (Forestier and
Lagier, 1971; Yagan and Khan, 1983). The
syndesmophytes of ankylosing spondylitis
are thin bridges through the anulus fribosus
from one vertebral body to the next, contrasting with the thick longitudinal ossification of DISH. Also, ankylosing spondylitis
mainly affects young adults as opposed to
the older age of onset in DISH. In both phenomena, the intervertebral space tends to be
maintained and both may present “whiskering” of the peripheral joints (Resnick et al.,
Reiter’s syndrome and psoriatic arthritis,
types of seronegative spondyloarthropathies, may also produce thin or thick paravertebral fusion, but overall this type of fusion parallels ankylosing spondylitis rather
than DISH (Rogers et al., 1985). Fluorosis
may also cause osteophytosis but periostitis
and sclerosis are more typical of fluorosis
(Ortner and Putschar, 1985). Ochronosis
and induced calcium pyrophosphate depositation disease, metabolic disorders, more
closely resemble ankylosing spondylitis
rather than DISH. Extensive intervertebral
disc ossification is typically present in
ochronosis (see Ortner and Putschar, 1985).
Fig. 1. Thoracic vertebrae of a Nubian male from the
Hypoparathyroidism, hypophosphatemia,
Semna South site showing the typical flowing ossification seen in DISH.
hypervitaminosis A, and healing fractures
are rare phenomena which can mimic DISH
(Forestier and Lagier, 1971; Resnick et al.,
(Fig. 1)sometimes called a “dripping candle 1978). Limitation of the phenomena to Nuwax” pattern (Forestier and Rotes-Querol, bian adults allows hypervitaminosis A to be
1950; Forestier and Lagier, 1971; Resnick ruled out.
et al., 1978; Resnick and Niwayama, 1981;
Rothschild, 1988).
The skeletal remains of 134 adult Meroitic
DISH in the past may have been confused
with ankylosing spondylitis. The apophy- Nubians from the Semna South site were
seal, costovertebral, and auricular surface of examined. The cemetery was excavated in
TABLE 1 . Most common synonyms for DISH or Diffuse
IdioDathic Skeletal Hwerostosis
2' ND C A T A R A C T
KM. I-
Fig. 2. The Wadi Halfa area of Sudan and surrounding localities (After Van Gerven, 1981).
1966-1968 in Northern Sudan, near the concentrated on the spine only. Sex was inNile region, 15 miles south of Wadi Halfa ferred from the size of the lumbar vertebrae,
(Fig. 2). Currently the skeletal remains from sacrum, and femoral head diameter, followSemna South are housed at the Anthropol- ing standard osteological techniques (Krogogy Department of Arizona State Univer- man and Iscan, 1986; Bass, 1987). Because
sity. The cultural association of these inhu- DISH is an age-dependent phenomenon,
mations corresponds to groups that based only the skeletons of mature adult individutheir economy on agriculture (Meriotic Pe- als were considered in the following analysis
riod, 350 B.C. to A.D. 350; Armelagos, 1977; and interpretations. No evidence of DISH
Van Gerven, 1981; Zabkar and Zabkar, was noted in younger individuals.
Research model
As DISH is a product of aging and as the
vertebrae manifest the pathognomonic features of the phenomenon, the present study
Eighteen cases (13.4%) of DISH were
identified among 134 adult Nubian spines
(Table 2). Diffuse idiopathic skeletal hyper-
TABLE 2. Specimens diagnosed as having DISH (based
on the Dresence o f Forestier’s disease)
Females (n = 56)
N 408-2
Males (n = 78)
N 201
N 228B
N 244
N 270
N 271
N 277
N 282
N 296-1
N 410
N 413
N 414
N 422-1
N 448-2
N 521
ostosis was found in 7% of the females while
males had 18%(Chi square = 3.3, P> 0.05).
Two males and one female had associated
seronegative spondyloarthropathies (SNS),
diagnosis based on the presence of irregular
and bulky vertebral ankylosing, apophyseal
fusion and periarticular erosions. Given the
high population frequency of DISH in this
Nubian sample, seronegative spondyloarthropathies could be anticipated to co-occur
in this population.
DISH in Nubians
The present study of Nubians shows
DISH was present in Africa as early as the
third century B.C. A 13.4% frequency of
DISH in these adult Nubians is high compared to other archaeological studies from
other areas, but lower than some modern
populations. Perhaps this high DISH prevalence in Nubians is due to sample bias during excavation or recovery. Although the authors were not involved in the excavation of
the Semna South site, to the best of our
knowledge the Nubian skeletons analyzed
represents a random sample. Arriaza (1993)
found 4% DISH in an approximately 4,000year-old sedentary fishing population from
northern Chile. Rogers et al. (1985)reported
a frequency of 2-3.7% DISH in a study of
Egyptian and European skeletons dating
from the twenty-first dynasty through A.D.
1850. For the Middle Ages, DISH has been
found to be as common (Kramar et al., 1990;
Waldron, 1985) as it is today for modern European populations. Using clinical data,
Julkunen et al. (1971,1975) reported a 3.8%
and 2.6% occurrence of DISH for modern
Finnish men and women over 40 years of
age, respectively. However, the frequencies
increased to 10% in individuals over 70
years of age. Rothschild and Woods (1991)
using the Todd collection (Cleveland Museum of Natural History) found DISH in
25% of men over age 65 while women had
only 4%.
There are three points about DISH which
have special anthropological importance: (1)
typically there is a late age of onset for
DISH; (2) there is differential sex distribution, with greater numbers of males affected; and (3) DISH has been associated
with high caloric intake, although this has
not been confirmed. These observations,
when related to the evidence of DISH in this
Nubian population, raise important issues
for consideration.
It is a popular belief that prehistoric peoples had shorter life spans than we do today.
If DISH is a phenomenon of old age and this
Nubian population had a significantly high
number of DISH cases, then did these Nubians generally live to advanced ages? Since
the skeletons were not always complete, biological age could not be used accurately to
reconstruct age of onset and demographic
distributions of this phenomenon in these
individuals. However, if we assume that
DISH has neither changed its virulence nor
the age of onset in the past 2,300 years, then
this Nubian population had life expectancies that were long enough to yield high frequencies of severe manifestations of DISH.
Some of the cases studied presented massive
ossification even in the cervical area. Although DISH may start as early as age 43
(Julkunen et al., 1971), it is interesting that
the prevalence definitely increases with age
in an almost exponential manner.
Why are females less affected by DISH?
This is possibly due to female bone gracility
and postmenopausal hormonal imbalances
that decrease the amount of bone formation.
Archaeologically and in modern clinical
cases, males, are more affected with DISH
than females. Therefore, upon finding a partial skeleton with much ossification due to
DISH, if the sex cannot be inferred by standard physical anthropology procedures,
then based on probability alone, the skeleton will most likely be a male.
Hajkova et al. (1965) and Julkunen et al.
(1971, 1975) have found that the frequency
of DISH increases with the presence of diabetes mellitus and obesity. However, the association of DISH and diabetes mellitus is
controversial. Resnick et al. (1978) and
Rothschild (1985) among others argued that
the studies showing association between
DISH and diabetes mellitus are inconclusive
because of the lack of standardized criteria
for glucose tolerance in individuals above 40
years of age. Rothschild (1985, 1988) suggested that the presence of DISH may be
advantageous, for instance, against neuroforamina1 narrowing.
Waldron (1985) found that nearly 10% of
the Medieval priest’s skeletons from Merton
Priory had DISH. He attributed this high
frequency to their gluttonous behavior. The
high prevalence of DISH observed in the Nubians from Semna South, whether related to
longevity o r obesity, needs further study.
Based on the late age of onset for DISH and
the hypothesis that diabetes and obesity
may cause predisposition to DISH, Arriaza
(1993) has postulated that DISH then
should be common in the higher ranks of
stratified prehistoric societies as compared
to hunter-gatherer populations. Arriaza
(1993) also theorized that DISH could be a
response to an evolutionary trend of increasing longevity; that is, DISH is the biological
response to excessive skeletal stress. Thus,
skeletal hyperostosis of the spine and appendicular skeleton may benefit the individual by providing extra strength to support a
weakened trunk and body, without a significant loss of mobility.
In summary, DISH is not just a product of
contemporaneous health disorders or modern human behavior; it has been present in
the Old World for more than 2,000 years. As
is the case in modern populations, DISH affected mostly males in ancient Nubia. DISH
is associated with less destructive processes
and much less pain than are the seronegative spondyloarthropathies. Patients with
DISH complain of spinal stiffness and mild
middle or lower back pain, but the condition
is often discovered when the patient is being
treated for other diseases typical of old age
(Forestier and Rotes-Querol, 1950; Resnick
et al., 1975). If DISH is the product of a
trend toward increasing longevity; that is, if
it is an age-adaptive phenomenon, then the
frequency of DISH should decrease as we
look back in time, and can be expected to
continue increasing in future populations.
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meroitic, diffuse, skeletal, idiopathic, semna, hyperostoses, suda, south, nubian
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